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Safe in the womb? Effects of air pollution to the unborn child and neonates

Abstract

Objective:

In this brief review, the authors focus on the effects of gestational exposures to urban air pollution on fetal development and neonatal outcomes.

Source of data:

In this review the authors used PubMed, Web of Science and SciELO research platforms, analyzing papers from the last 30 years.

Summary of the findings:

Epidemiological and experimental evidence agree that gestational exposure to air pollution in urban increases the risks for low birth weight, preterm birth, congenital malformation, intrauterine growth restriction, and neonatal mortality. Furthermore, exposures are associated with increased risks for preeclampsia, hypertension, gestational diabetes.

Conclusions:

Therefore, it is time for greater involvement and engagement of the health sector in the discussion of public policies that may affect the quality of the environment, and that directly or indirectly impact the health of those who were not yet born.

KEYWORDS
Air pollution; Pregnancy; Fetal development

Introduction

The first evidence of the relationship between exposure to environmental pollution and reproductive effects were derived from observational studies of unintentionally exposed wildlife.11 Guillette Jr LJ, Edwards TM. Environmental influences on fertility: can we learn lessons from studies of wildlife? Fertil Steril. 2008;89:e21–4. The reproductive process is subject to toxic effects from a variety of substances present in the environment, particularly anthropogenic contaminants, including agrochemicals, traffic-derived air pollutants, and industrial wastes.22 Stillerman KP, Mattison DR, Giudice LC, Woodruff TJ. Environmental exposures and adverse pregnancy outcomes: a review of the science. ReprodSci. 2008;15:631–50.

In the last 3 decades, numerous studies have been published showing that environmental air pollutants that the authors have contact with in daily life affect reproductive health and, in particular, produce adverse effects on fertility, pregnancy outcomes, fetal health, and development.33 Woodruff TK, Walker CL. Fetal and early postnatal environmental exposures and reproductive health effects in the female. Fertil Steril. 2008;89:e47–51.,44 Maisonet M, Correa A, Misra D, Jaakkola JJ. A review of the literature on the effects of ambient air pollution on fetal growth. Environ Res. 2004;95:106–15.,55 Johnson NM, Hoffmann AR, Behlen JC, Lau C, Pendleton D, Harvey N, et al. Air pollution and children's health-a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter. Environ Health PrevMed. 2021;26:72.

In addition to immediately observable gestational outcomes, such as low birth weight, IUGR, neonatal mortality, the authors must not forget that any perturbation that occurs during an intrauterine period of life is determinant not only for fetal development but also can predispose individuals to later life diseases.66 Gluckman PD, Hanson MA, Spencer HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005;20: 527–33.

From their early stages of development, still in the womb, children are one of the most sensitive groups to air pollution. Children breathe more air per kilogram of body weight, they spend more time in outdoor activities significantly increasing their exposure dose. Moreover, as they have a longer life expectancy, they would have more time to develop health problems resulting from exposures that occurred earlier.

According to the World Health Organization (WHO), 1.7 million children under the age of 5 have died worldwide from diseases and conditions related to the environment, including air pollution, non-drinking water, poor sanitation, and hygiene or exposure to toxic chemicals. Air pollution (AP), a widespread environmental contaminant and causes approximately 600 000 deaths in children under 5 years annually and increases the risk for respiratory infections, asthma, and adverse neonatal conditions.77 World Health Organization (WHO). Don’t pollute my future! The impact of the environment on children’s health. Geneva: WHO; 2017.

Science and health authorities have been warning for a long time about the harmful effects that air pollution can have on people's health, and the impacts can range from minor transient irritation to the eyes and throat, breathing difficulties to death from cardiorespiratory problems and lung cancer. The outcome will depend on some factors, the authors highlight the two most important: age and exposure dose. And despite the development of cleaner technologies in the energetic and transport sector, the problem of air pollution seems to be far from solved.

In this brief review, the authors focus on the effects of gestational exposures to urban air pollution on fetal development and neonatal outcomes.

Urban air pollution

Urban air pollution, which is derived largely from combustion processes of fossil fuels (vehicle emissions), is a mixture containing many toxic components which include carbon monoxide (CO), nitrogen dioxide (NO2), Sulphur dioxide (SO2), ozone (O3), lead (Pb), polycyclic aromatic hydrocarbons (PAH) and particulate matter (PM). Particulate matter is a complex mixture of microscopic particles and liquid droplets composed of nitrates, sulfates, organic substances (e.g. polycyclic aromatic hydrocarbons), metals (e.g. cadmium, Pb), and dust particles.88 World Health Organization (WHO). WHO global air quality guidelines: particulate matter (PM2.5 and PM10), ozone, nitrogen dioxide, sulfur dioxide and carbono monoxide. Geneva: WHO; 2021. Particles are classified according to their size in PM10 and PM2.5, which means that these particles have diameters of 10 and 2.5 micrometers, respectively. If the authors compare the size of PM2.5 to a grain of sand or to an erythrocyte, they are 40 times and 3 times bigger than PM2.5, respectively.99 Siciliano B, Dantas G, Silva CM, Arbilla G. The Updated Brazilian National Air Quality Standards: A Critical Review. J. Braz. Chem Soc. 2020;31:523–35.

Among the main pollutants mentioned above, particulate matter is the most harmful to health due to its small size and its characteristic of adsorbing other toxic agents on its surface. These particles can translocate almost all physiological barriers (e.g. alveolar-capillary barrier, blood-brain barriers, dermal barrier, maternal-fetal interface.1010 Bové H, Bongaerts E, Slenders E, Bijnens EM, Saenen ND, Gyselaers W, et al. Ambient black carbon particles reach the fetal side of human placenta. Nat Commun. 2019;10:3866.,1111 Oberdörster G, Sharp Z, Atudorei V, Elder A, Gelein R, Kreyling W, et al. Translocation of inhaled ultrafine particles to the brain. Inhal Toxicol. 2004;16:437–45.,1212 Schneider M, Stracke F, Hansen S, Schaefer UF. Nanoparticles and their interactions with the dermal barrier. Dermatoendocrinol. 2009;1:197–206.,1313 Yang W, Peters JI, Williams 3rd RO. Inhaled nanoparticles–a current review. Int J Pharm. 2008;356:239–47.

Air quality is determined by the concentration of criteria pollutants that are measured daily. There are defined limits for each pollutant and the acceptable values vary depending on the environmental authority that has defined them. These levels are determined by the health risks associated with them and by public health relevance. WHO has an air quality guideline that recommends levels for 6 pollutants – PM10, PM 2.5, O3, NO2, SO2, and CO.88 World Health Organization (WHO). WHO global air quality guidelines: particulate matter (PM2.5 and PM10), ozone, nitrogen dioxide, sulfur dioxide and carbono monoxide. Geneva: WHO; 2021. In Brazil, standard limits are defined by the National Environment Council of Brazil (CONAMA)1414 Brasil. Órgão: Ministério do Meio Ambiente/Conselho Nacional do Meio Ambiente. Resolução n.° 491, de 19 de novembro de 2018. Dispöe sobre padröes de qualidade do ar [accessed 6 oct. 2021]. Available from: https://www.in.gov.br/web/guest/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/51058895/do1-2018-11-21-resolucao-n-491-de-19-de-novembro-de-2018-51058603.
https://www.in.gov.br/web/guest/materia/...
and Sao Paulo State has its local standard,1515 São Paulo. Assembleia Legislativa do Estado de São Paulo. Decreto n° 59.113, de 23 de abril de 2013. Estabelece novos padrões de qualidade do ar e dá providências correlatas accessed 6 Oct. 2021]. Available from: https://www.al.sp.gov.br/repositorio/legislacao/decreto/2013/decreto-59113-23.04.2013.html
https://www.al.sp.gov.br/repositorio/leg...
which is very similar to those established by the CONAMA. It is important to note that the study’s tstandard is less stringent than the WHO’s posing greater risks to the population’s health.99 Siciliano B, Dantas G, Silva CM, Arbilla G. The Updated Brazilian National Air Quality Standards: A Critical Review. J. Braz. Chem Soc. 2020;31:523–35. Table 1 depicts the current mean 24hs limits for the criteria pollutants defined by WHO, CONAMA and Environmental Company of the State of São Paulo (CETESB).

Table 1
Limits of the daily mean concentration of criteria pollutants according to the air quality guidelines from WHO, CONAMA (national standards, Brazil), and CETESB (São Paulo State, Brazil).

Negative effects of gestational exposure to air pollution

Respiratory and cardiovascular diseases are the most commonly observed and studied effects associated with exposure to air pollution followed by neoplasia. However, in the last two decades, lesser-known effects have been linked to chronic exposures to air pollution including adverse reproductive outcomes, neurodegenerative diseases and metabolic disorders.1616 Manisalidis I, Stavropoulou E, Stavropoulos A, Bezirtzoglou E. Environmental and Health Impacts of Air Pollution: A Review. Front Public Health. 2020;8:14.

Special attention has been given to gestational exposures since these early exposures can predispose to other negative outcomes later in adult life, such as cardiovascular disease, stroke, chronic respiratory disease, diabetes and cancer.

The earliest published evidence of negative health effects on children was published in the 1970s and showed an association between exposure to industrial air pollution and infant mortality.1717 Collins JJ, Kasap HS, Holland WW. Environmental factors in child mortality in England and Wales. Am J Epidemiol. 1971;93:10–22.,1818 Lave LB, Seskin EP. Air Pollution and Human Health. Baltimore, MD: Johns Hopkins University Press; 1977. However, it was only in the 1990s that new studies were published evaluating this issue in more detail and with a greater focus on prenatal exposures.

Studies conducted in Europe, Asia, and the Americas agree that expectant mothers exposed to environmental levels of air pollution are at greater risk of having the development of their pregnancy compromised and maternal and fetal health could be affected. However, it is not clear until now whether the effects are due to a specific pollutant or to the interactions of different pollutants and nor if pre-gestational exposure could aggravate the effects.

The main effects observed in epidemiological studies as a result of gestational exposure to pollution are low birth weight (LBW), intrauterine growth restriction (IUGR), prematurity, congenital malformations, and neonatal mortality.1919 Backes CH, Nelin T, Gorr MW, Wold LE. Early life exposure to air pollution: how bad is it? Toxicol Lett. 2013;216:47–53.,2020 Srám RJ, Binkova B, Dejmek J, Bobak M. Ambient air pollution and pregnancy outcomes: a review of the literature. Environ Health Perspect. 2005;113:375–82.

Meta-analysis results estimated that for every 10 μg/m3 increase in PM2.5 birth weight is reduced from −15.9 to −23.4 g. When analyzed, which trimesters are determinant for these effects, results are different, however, the critical windows of susceptibility seem to be the last third trimester.2121 Stieb DM, Chen L, Eshoul M, Judek S. Ambient air pollution, birth weight and preterm birth: a systematic review and metaanalysis. Environ Res. 2012;117:100–11.,2222 Sun M, Yan W, Fang K, Chen D, Liu J, Chen Y, et al. The correlation between PM2.5 exposure and hypertensive disorders in pregnancy: A Meta-analysis. Sci Total Environ. 2020;703:134985.,2323 Zhu X, Liu Y, Chen Y, Yao C, Che Z, Cao J. Maternal exposure to fine particulate matter (PM2.5) and pregnancy outcomes: a meta-analysis. Environ Sci Pollut Res Int. 2015;22:3383–96.,2424 Lamichhane DK, Leem JH, Lee JY, Kim HC. A meta-analysis of exposure to particulate matter and adverse birth outcomes. Environ Health Toxicol. 2015;30:e2015011. Greater risks for preterm birth seems also to be related to exposure in the 3rd trimester, DeFranco et al.2525 DeFranco E, Moravec W, Xu F, Hall E, Hossain M, Haynes EN, et al. Exposure to airborne particulate matter during pregnancy is associated with preterm birth: a population-based cohort study. Environ Health. 2016;15:6. found a 19% increased risk of PTB.

Intrauterine and neonatal mortality and preterm birth44 Maisonet M, Correa A, Misra D, Jaakkola JJ. A review of the literature on the effects of ambient air pollution on fetal growth. Environ Res. 2004;95:106–15.,2626 Glinianaia SV, Rankin J, Bell R, Pless-Mulloli T, Howel D. Particulate air pollution and fetal health: a systematic review of the epidemiologic evidence. Epidemiology. 2004;15:36–45. are outcomes less frequently associated with gestational exposure to air pollution.

More recently, new effects associated with gestational exposure were evidenced, such as preeclampsia,2222 Sun M, Yan W, Fang K, Chen D, Liu J, Chen Y, et al. The correlation between PM2.5 exposure and hypertensive disorders in pregnancy: A Meta-analysis. Sci Total Environ. 2020;703:134985.,2727 Hu H, Ha S, Roth J, Kearney G, Talbott EO, Xu X. Ambient Air Pollution and Hypertensive Disorders of Pregnancy: A Systematic Review and Meta-analysis. Atmos Environ (1994). 2014;97:336–45. hypertension and gestational diabetes,2828 Fleisch AF, Gold DR, Rifas-Shiman SL, Koutrakis P, Schwartz JD, Kloog I, et al. Air pollution exposure and abnormal glucose tolerance during pregnancy: the project Viva cohort. Environ Health Perspect. 2014;122:378–83.,2929 Fleisch AF, Kloog I, Luttmann-Gibson H, Gold DR, Oken E, Schwartz JD. Air pollution exposure and gestational diabetes mellitus among pregnant women in Massachusetts: a cohort study. Environ Health. 2016;15:40.,3030 Lu MC, Wang P, Cheng TJ, Yang CP, Yan YH. Association of temporal distribution of fine particulate matter with glucose homeostasis during pregnancy in women of Chiayi City. Taiwan. Environ Res. 2017;152:81–7. placental abruption,3131 Michikawa T, Morokuma S, Yamazaki S, Fukushima K, Kato K, Nitta H. Exposure to air pollutants during the early weeks of pregnancy, and placenta praevia and placenta accreta in the western part of Japan. Environ Int. 2016;92-93:464–70. premature rupture of membranes,3232 Wallace ME, Grantz KL, Liu D, Zhu Y, Kim SS, Mendola P. Exposure to Ambient Air Pollution and Premature Rupture of Membranes. Am J Epidemiol. 2016;183:1114–21. placenta praevia, and accrete.3333 Michikawa T, Morokuma S, Yamazaki S, Fukushima K, Kato K, Nitta H. Air Pollutant Exposure Within a Few Days of Delivery and Placental Abruption in Japan. Epidemiology. 2017;28: 190–6.

A meta-analysis conducted by Pedersen et al.3434 Pedersen M, Stayner L, Slama R, Sørensen M, Figueras F, Nieuwenhuijsen MJ, et al. Ambient air pollution and pregnancyinduced hypertensive disorders: a systematic review and metaanalysis. Hypertension. 2014;64:494–500. have shown that maternal exposure to 5 μg/m3 increments in ambient PM2.5 is associated with a 50% increased odds of pregnancy-induced hypertension and preeclampsia.

Fetal developmental disruptions may occur indirectly (maternally mediated), as a result of direct effects on the fetus, or can be a consequence of the combination of both. In most cases, embryo/fetal toxicity occurs via maternal exposure to toxic agents but the authors must keep in mind that male exposure to contaminants may be teratogenic or impair gestation if the chromosomes of the spermatozoa are damaged.3535 Trasler JM, Doerksen T. Teratogen update: paternal exposures-reproductive risks. Teratology. 1999;60:161–72. There is also evidence of paternally mediated effects of air pollution on the risk of adverse health outcomes in offspring. However, the effects of the father's exposure on the health of his offspring are beyond the scope of this review.3636 Braun JM, Messerlian C, Hauser R. Fathers Matter: Why It's Time to Consider the Impact of Paternal Environmental Exposures on Children's Health. Curr Epidemiol Rep. 2017;4:46–55.,3737 Rubes J, Selevan SG, Evenson DP, Zudova D, Vozdova M, Zudova Z, et al. Episodic air pollution is associated with increased DNA fragmentation in human sperm without other changes in semen quality. Hum Reprod. 2005;20:2776–83.,3838 Selevan SG, Borkovec L, Slott VL, Zudová Z, Rubes J, Evenson DP, et al. Semen quality and reproductive health of young Czech men exposed to seasonal air pollution. Environ Health Perspect. 2000;108:887–94.

Low birth weight is a predominant effect associated with exposure to ambient air pollution. Birth weight is an important indicator of subsequent health issues; low-birth-weight babies are more prone to develop hypertension, coronary heart disease, and non-insulin-dependent diabetes during adulthood.3939 Osmond C, Barker DJ. Fetal, infant, and childhood growth are predictors of coronary heart disease, diabetes, and hypertension in adult men and women. Environ Health Perspect. 2000;108:545–53. Jedrychowski et al.4040 Jedrychowski W, Bendkowska I, Flak E, Penar A, Jacek R, Kaim I, et al. Estimated risk for altered fetal growth resulting from exposure to fine particles during pregnancy: an epidemiologic prospective cohort study in Poland. Environ Health Perspect. 2004;112:1398–402. observed that not only birth weight is affected, changes in other anthropometric measurements can be observed, such as reduction in head circumference. Studies conducted by van den Hoove et al.4141 van den Hooven EH, Pierik FH, de Kluizenaar Y, Willemsen SP, Hofman A, van Ratingen SW, et al. Air pollution exposure during pregnancy, ultrasound measures of fetal growth, and adverse birth outcomes: a prospective cohort study. Environ Health Perspect. 2012;120:150–6. using ultrasound measurements observed that fetal growth is compromised by maternal exposure to air pollution. In this study, NO2 levels were inversely associated with fetal femur length in the second and third trimester, and PM10 and NO2 levels both were associated with smaller fetal head circumference in the third trimester.

Baïz et al.,4242 Baïz N, Slama R, Béné MC, Charles MA, Kolopp-Sarda MN, Magnan A, et al. Maternal exposure to air pollution before and during pregnancy related to changes in newborn's cord blood lymphocyte subpopulations. The EDEN study cohort. BMC Pregnancy Childbirth. 2011;11:87. found that maternal exposure to ambient urban levels of NO2 and PM10 during the whole pregnancy was a strong predictor of low vitamin D status in newborns. In other studies, it was observed that maternal exposure during pregnancy affects the distribution of NK, T lymphocytes in and IgE content of umbilical blood.4343 Dostál M, Hertz-Picciotto I, Wegienka G, Dejmek J, Skokanová V, Srám RJ. Parameters of cellular immunity in maternal and umbilical cord blood in relation to air pollution. Preliminary results of a pregnancy outcomes study. Cas Lek Cesk. 2000; 139:183–8.,4444 Herr CE, Dostal M, Ghosh R, Ashwood P, Lipsett M, Pinkerton KE, et al. Air pollution exposure during critical time periods in gestation and alterations in cord blood lymphocyte distribution: a cohort of livebirths. Environ Health. 2010;9:46. The consequences of gestational exposure on lung development and childhood pulmonary function have also been reported.4545 Wright RJ, Brunst KJ. Programming of respiratory health in childhood: influence of outdoor air pollution. Curr Opin Pediatr. 2013;25:232–9.

Different studies point out that diverse congenital deformities could be associated with maternal exposure to air pollutants. A recent meta-analysis was conducted for several combinations of air pollutants and congenital defects and reported that NO2 and PM2.5 were associated with the risk of pulmonary valve stenosis with OR = 1.74 and OR = 1.42 respectively. The risk of developing tetralogy of Fallot (TOF) was observed to be associated with PM2.5 with OR = 1.52. SO2 exposure was related to a high risk of the ventricular septal defect (VSD) with OR = 1.15 and orofacial defects (OR = 1.27).4646 Ravindra K, Chanana N, Mor S. Exposure to air pollutants and risk of congenital anomalies: A systematic review and metaanalysis. Sci Total Environ. 2021;765:142772.

Despite the adoption of different study designs and statistical evaluations, and the presence of confounding variables (e.g. maternal smoking, gestational age, and socioeconomic factors), most of these investigations suggest that the reported associations are causal. Studies conducted using animal models give support to the epidemiological findings.55 Johnson NM, Hoffmann AR, Behlen JC, Lau C, Pendleton D, Harvey N, et al. Air pollution and children's health-a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter. Environ Health PrevMed. 2021;26:72.

Mechanisms

There are many proposed mechanisms to explain how the noxious substances present in air pollution might interfere adversely in gestation.

Kannan et al.4747 Kannan S, Misra DP, Dvonch JT, Krishnakumar A. Exposures to airborne particulate matter and adverse perinatal outcomes: a biologically plausible mechanistic framework for exploring potential effect modification by nutrition. Environ Health Perspect. 2006;114:1636–42. suggest a number of plausible biological mechanisms by which particulate matter would influence the development of pregnancy increases the risks of negative outcomes such as low birth weight. They proposed that exposure would increase oxidative stress and trigger systemic maternal inflammation, increase blood pressure, and impairments in endothelial function which negatively impact placental nutrient and oxygen transport functions.

Among the pollutants present in the complex mixture (CO, SO2, NOx, MP, O3, PAH) that constitute air pollution, it is only known how CO exerts its effects on the fetus. The mechanisms by which other pollutants influence fetal development remain unclear. It is possible that DNA damage, as well as the activation of P450 enzymes, endocrine alterations are involved, compromising placental function. The present study’s research group has pioneered the experimental investigation of the impacts of exposure to particulate matter on placental and fetal development. Using exposure chambers receiving ambient air from a region of intense vehicular traffic in the city of São Paulo and filtered air, the authors showed that morpho-functional alterations of the placenta are really involved in the impairment of fetal development assessed by birth weight.4848 Veras MM, Damaceno-Rodrigues NR, Caldini EG, Maciel Ribeiro AA, Mayhew TM, Saldiva PH, et al. Particulate urban air pollution affects the functional morphology of mouse placenta. Biol Reprod. 2008;79:578–84.,4949 Veras MM, Damaceno-Rodrigues NR, Guimarães Silva RM, Scoriza JN, Saldiva PH, Caldini EG, et al. Chronic exposure to fine particulate matter emitted by traffic affects reproductive and fetal outcomes in mice. Environ Res. 2009;109:536–43. Furthermore, exposure during pregnancy to PM2.5 lowers placental concentrations of the angiogenic factors VEGF and FLK-1 (receptors for a vascular endothelial growth factor (VEGF).5050 Soto SF, Melo JO, Marchesi GD, Lopes KL, Veras MM, Oliveira IB, et al. Exposure to fine particulate matter in the air alters placental structure and the renin-angiotensin system. PLoS One. 2017;12:e0183314.

Uncertainties

All of the published reviews acknowledged that there are many uncertainties on the association between gestational exposure to air pollution and negative outcomes, such as limited information on personal exposures and difficulties in linking particulate matter (PM) composition or single component to the effects and to control confounding factors Undoubtedly these aspects point out that there is still a need of further toxicological and clinical studies.

Even though, these findings are important to serve as a guide for further studies and to generate questions that need to be answered:

  • - Which trimester of pregnancy is more relevant to the impairment of fetal development?

  • - Which component of the PM presents a higher risk for reduced birth weight and other outcomes?

  • - Could multigenerational exposure to ambient PM concentration present cumulative effects?

There must also increase de number of studies on the effects of air pollution generated by wildfires and agricultural fires, as in recent years the authors have seen numerous events of large proportions that certainly impacted the health of pregnant women, newborns, and children.

Conclusion and future directions

In urban areas, exposure to air pollution is unavoidable. If the authors consider that half of the global population lives in urban areas, most of these areas have moderate to high levels of air pollution, prenatal exposure to air pollution increases the risk for LBW and IUGR, and that these outcomes are related to greater risks for hypertension, diabetes and metabolic disorders later in life, the impact of air pollution on the health status of the next generations will be of great concern. Therefore, it is time for greater involvement and engagement of the health sector in the discussion of public policies that may affect the quality of the environment and directly or indirectly negatively impact the health of those who were not yet born.

References

  • 1
    Guillette Jr LJ, Edwards TM. Environmental influences on fertility: can we learn lessons from studies of wildlife? Fertil Steril. 2008;89:e21–4.
  • 2
    Stillerman KP, Mattison DR, Giudice LC, Woodruff TJ. Environmental exposures and adverse pregnancy outcomes: a review of the science. ReprodSci. 2008;15:631–50.
  • 3
    Woodruff TK, Walker CL. Fetal and early postnatal environmental exposures and reproductive health effects in the female. Fertil Steril. 2008;89:e47–51.
  • 4
    Maisonet M, Correa A, Misra D, Jaakkola JJ. A review of the literature on the effects of ambient air pollution on fetal growth. Environ Res. 2004;95:106–15.
  • 5
    Johnson NM, Hoffmann AR, Behlen JC, Lau C, Pendleton D, Harvey N, et al. Air pollution and children's health-a review of adverse effects associated with prenatal exposure from fine to ultrafine particulate matter. Environ Health PrevMed. 2021;26:72.
  • 6
    Gluckman PD, Hanson MA, Spencer HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005;20: 527–33.
  • 7
    World Health Organization (WHO). Don’t pollute my future! The impact of the environment on children’s health. Geneva: WHO; 2017.
  • 8
    World Health Organization (WHO). WHO global air quality guidelines: particulate matter (PM2.5 and PM10), ozone, nitrogen dioxide, sulfur dioxide and carbono monoxide. Geneva: WHO; 2021.
  • 9
    Siciliano B, Dantas G, Silva CM, Arbilla G. The Updated Brazilian National Air Quality Standards: A Critical Review. J. Braz. Chem Soc. 2020;31:523–35.
  • 10
    Bové H, Bongaerts E, Slenders E, Bijnens EM, Saenen ND, Gyselaers W, et al. Ambient black carbon particles reach the fetal side of human placenta. Nat Commun. 2019;10:3866.
  • 11
    Oberdörster G, Sharp Z, Atudorei V, Elder A, Gelein R, Kreyling W, et al. Translocation of inhaled ultrafine particles to the brain. Inhal Toxicol. 2004;16:437–45.
  • 12
    Schneider M, Stracke F, Hansen S, Schaefer UF. Nanoparticles and their interactions with the dermal barrier. Dermatoendocrinol. 2009;1:197–206.
  • 13
    Yang W, Peters JI, Williams 3rd RO. Inhaled nanoparticles–a current review. Int J Pharm. 2008;356:239–47.
  • 14
    Brasil. Órgão: Ministério do Meio Ambiente/Conselho Nacional do Meio Ambiente. Resolução n.° 491, de 19 de novembro de 2018. Dispöe sobre padröes de qualidade do ar [accessed 6 oct. 2021]. Available from: https://www.in.gov.br/web/guest/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/51058895/do1-2018-11-21-resolucao-n-491-de-19-de-novembro-de-2018-51058603
    » https://www.in.gov.br/web/guest/materia/-/asset_publisher/Kujrw0TZC2Mb/content/id/51058895/do1-2018-11-21-resolucao-n-491-de-19-de-novembro-de-2018-51058603
  • 15
    São Paulo. Assembleia Legislativa do Estado de São Paulo. Decreto n° 59.113, de 23 de abril de 2013. Estabelece novos padrões de qualidade do ar e dá providências correlatas accessed 6 Oct. 2021]. Available from: https://www.al.sp.gov.br/repositorio/legislacao/decreto/2013/decreto-59113-23.04.2013.html
    » https://www.al.sp.gov.br/repositorio/legislacao/decreto/2013/decreto-59113-23.04.2013.html
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    Manisalidis I, Stavropoulou E, Stavropoulos A, Bezirtzoglou E. Environmental and Health Impacts of Air Pollution: A Review. Front Public Health. 2020;8:14.
  • 17
    Collins JJ, Kasap HS, Holland WW. Environmental factors in child mortality in England and Wales. Am J Epidemiol. 1971;93:10–22.
  • 18
    Lave LB, Seskin EP. Air Pollution and Human Health. Baltimore, MD: Johns Hopkins University Press; 1977.
  • 19
    Backes CH, Nelin T, Gorr MW, Wold LE. Early life exposure to air pollution: how bad is it? Toxicol Lett. 2013;216:47–53.
  • 20
    Srám RJ, Binkova B, Dejmek J, Bobak M. Ambient air pollution and pregnancy outcomes: a review of the literature. Environ Health Perspect. 2005;113:375–82.
  • 21
    Stieb DM, Chen L, Eshoul M, Judek S. Ambient air pollution, birth weight and preterm birth: a systematic review and metaanalysis. Environ Res. 2012;117:100–11.
  • 22
    Sun M, Yan W, Fang K, Chen D, Liu J, Chen Y, et al. The correlation between PM2.5 exposure and hypertensive disorders in pregnancy: A Meta-analysis. Sci Total Environ. 2020;703:134985.
  • 23
    Zhu X, Liu Y, Chen Y, Yao C, Che Z, Cao J. Maternal exposure to fine particulate matter (PM2.5) and pregnancy outcomes: a meta-analysis. Environ Sci Pollut Res Int. 2015;22:3383–96.
  • 24
    Lamichhane DK, Leem JH, Lee JY, Kim HC. A meta-analysis of exposure to particulate matter and adverse birth outcomes. Environ Health Toxicol. 2015;30:e2015011.
  • 25
    DeFranco E, Moravec W, Xu F, Hall E, Hossain M, Haynes EN, et al. Exposure to airborne particulate matter during pregnancy is associated with preterm birth: a population-based cohort study. Environ Health. 2016;15:6.
  • 26
    Glinianaia SV, Rankin J, Bell R, Pless-Mulloli T, Howel D. Particulate air pollution and fetal health: a systematic review of the epidemiologic evidence. Epidemiology. 2004;15:36–45.
  • 27
    Hu H, Ha S, Roth J, Kearney G, Talbott EO, Xu X. Ambient Air Pollution and Hypertensive Disorders of Pregnancy: A Systematic Review and Meta-analysis. Atmos Environ (1994). 2014;97:336–45.
  • 28
    Fleisch AF, Gold DR, Rifas-Shiman SL, Koutrakis P, Schwartz JD, Kloog I, et al. Air pollution exposure and abnormal glucose tolerance during pregnancy: the project Viva cohort. Environ Health Perspect. 2014;122:378–83.
  • 29
    Fleisch AF, Kloog I, Luttmann-Gibson H, Gold DR, Oken E, Schwartz JD. Air pollution exposure and gestational diabetes mellitus among pregnant women in Massachusetts: a cohort study. Environ Health. 2016;15:40.
  • 30
    Lu MC, Wang P, Cheng TJ, Yang CP, Yan YH. Association of temporal distribution of fine particulate matter with glucose homeostasis during pregnancy in women of Chiayi City. Taiwan. Environ Res. 2017;152:81–7.
  • 31
    Michikawa T, Morokuma S, Yamazaki S, Fukushima K, Kato K, Nitta H. Exposure to air pollutants during the early weeks of pregnancy, and placenta praevia and placenta accreta in the western part of Japan. Environ Int. 2016;92-93:464–70.
  • 32
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Publication Dates

  • Publication in this collection
    20 Apr 2022
  • Date of issue
    Mar-Apr 2022

History

  • Received
    26 Sept 2021
  • Accepted
    27 Sept 2021
  • Published
    03 Nov 2021
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